Endogenous hydrogen sulphide mediates the cardioprotection induced by ischemic postconditioning

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 295, Issue 3, 2008, Pages

  Yong, Qian Chen ^a   Lee, Shiau Wei ^a   Foo, Chun Shin ^a   Neo, Kay Li ^a   Chen, Xin ^a   Bian, Jin Song ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Akt; Endothelial nitric oxide synthase; Hydrogen sulphide; Protein kinase C

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CHELERYTHRINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROGEN SULFIDE; PROPARGYLGLYCINE; PROTEIN KINASE B; PROTEIN KINASE C ALPHA; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; ALKYNE; BLOCKING ANTIBODY; CHROMONE DERIVATIVE; DIMETHYL SULFOXIDE; DRUG DERIVATIVE; GLYCINE; IMMUNOGLOBULIN G; ISOENZYME; MORPHOLINE DERIVATIVE; ONCOPROTEIN; PROTEIN KINASE C;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HEART FUNCTION; HEART INFARCTION; HEART INFARCTION SIZE; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PERFORMANCE; HEART PROTECTION; ISCHEMIC POSTCONDITIONING; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; ANIMAL; BLOOD PRESSURE; DRUG ANTAGONISM; DRUG EFFECT; ELECTROCARDIOGRAPHY; ENZYMOLOGY; HEART DISEASE; HEART LEFT VENTRICLE FUNCTION; IN VITRO STUDY; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SPRAGUE DAWLEY RAT;

ALKYNES; ANIMALS; ANTIBODIES, BLOCKING; BLOOD PRESSURE; CHROMONES; DIMETHYL SULFOXIDE; ELECTROCARDIOGRAPHY; ENZYME ACTIVATION; GLYCINE; HEART DISEASES; HYDROGEN SULFIDE; IMMUNOGLOBULIN G; ISOENZYMES; MALE; MORPHOLINES; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; NITRIC OXIDE SYNTHASE TYPE III; ONCOGENE PROTEIN V-AKT; PHOSPHORYLATION; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; VENTRICULAR FUNCTION, LEFT;

EID: 54049110077     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00244.2008     Document Type: Article

References (62)

1. Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16: 1066-1071, 1996.
2. Bian JS, Yong QC, Pan TT, Feng ZN, Ali MY, Zhou S, Moore PK. Role of hydrogen sulfide in the cardioprotection caused by ischemic preconditioning in the rat heart and cardiac myocytes. J Pharmacol Exp Ther 316: 670-678, 2006.
3. Bliksoen M, Kaljusto ML, Vaage J, Stenslokken KO. Effects of hydrogen sulphide on ischaemia-reperfusion injury and ischaemic preconditioning in the isolated, perfused rat heart. Eur J Cardiothorac Surg 34: 344-349, 2008.
4. Chen P, Poddar R, Tipa EV, Dibello PM, Moravec CD, Robinson K, Green R, Kruger WD, Garrow TA, Jacobsen DW. Homocysteine metabolism in cardiovascular cells and tissues: implications for hyperhomocysteinemia and cardiovascular disease. Adv Enzyme Regul 39: 93-109, 1999.
5. Crisostomo PR, Wang M, Wairiuko GM, Terrell AM, Meldrum DR. Postconditioning in females depends on injury severity. J Surg Res 134: 342-347, 2006.
6. Darling CE, Jiang R, Maynard M, Whittaker P, Vinten-Johansen J, Przyklenk K. Postconditioning via stuttering reperfusion limits myocardial infarct size in rabbit hearts: role of ERK1/2. Am J Physiol Heart Circ Physiol 289: H1618-H1626, 2005.
7. ATP channels. J Pharmacol Exp Ther 316: 325-335, 2006.
8. Dombkowski RA, Russell MJ, Olson KR. Hydrogen sulfide as an endogenous regulator of vascular smooth muscle tone in trout. Am J Physiol Regul Integr Comp Physiol 286: R678-R685, 2004.
9. Dombkowski RA, Russell MJ, Schulman AA, Doellman MM, Olson KR. Vertebrate phylogeny of hydrogen sulfide vasoactivity. Am J Physiol Regul Integr Comp Physiol 288: R243-R252, 2005.
10. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, Jiao X, Scalia R, Kiss L, Szabo C, Kimura H, Chow CW, Lefer DJ. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci USA 104: 15560-15565, 2007.
11. Fantinelli JC, Mosca SM. Comparative effects of ischemic pre and postconditioning on ischemia-reperfusion injury in spontaneously hypertensive rats (SHR). Mol Cell Biochem 296: 45-51, 2007.
12. Geng B, Chang L, Pan C, Qi Y, Zhao J, Pang Y, Du J, Tang C. Endogenous hydrogen sulfide regulation of myocardial injury induced by isoproterenol. Biochem Biophys Res Commun 318: 756-763, 2004.
13. 2S generated by heart in rat and its effects on cardiac function. Biochem Biophys Res Commun 313: 362-368, 2004.
14. Hausenloy DJ, Tsang A, Mocanu MM, Yellon DM. Ischemic preconditioning protects by activating prosurvival kinases at reperfusion. Am J Physiol Heart Circ Physiol 288: H971-H976, 2005.
15. Hu X, Li T, Bi S, Jin Z, Zhou G, Bai C, Li L, Cui Q, Liu W. Possible role of hydrogen sulfide on the preservation of donor rat hearts. Transplant Proc 39: 3024-3029, 2007.
16. Hu Y, Chen X, Pan TT, Neo KL, Lee SW, Khin ES, Moore PK, Bian JS. Cardioprotection induced by hydrogen sulfide preconditioning involves activation of ERK and PI3K/Akt pathways. Pflügers Arch 455: 607-616, 2008.
17. 2S in patients with coronary heart disease. [In Chinese.] Di Yi Jun Yi Da Xue Xue Bao 25: 951-954, 2005.
18. ATP channels. Basic Res Cardiol 101: 53-60, 2006.
19. Kimura Y, Kimura H. Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18: 1165-1167, 2004.
20. Kin H, Zatta AJ, Lofye MT, Amerson BS, Halkos ME, Kerendi F, Zhao ZQ, Guyton RA, Headrick JP, Vinten-Johansen J. Postconditioning reduces infarct size via adenosine receptor activation by endogenous adenosine. Cardiovasc Res 67: 124-133, 2005.
21. Kin H, Zhao ZQ, Sun HY, Wang NP, Corvera JS, Halkos ME, Kerendi F, Guyton RA, Vinten-Johansen J. Postconditioning attenuates myocardial ischemia-reperfusion injury by inhibiting events in the early minutes of reperfusion. Cardiovasc Res 62: 74-85, 2004.
22. Lee SW, Cheng Y, Moore PK, Bian JS. Hydrogen sulphide regulates intracellular pH in vascular smooth muscle cells. Biochem Biophys Res Commun 358: 1142-1147, 2007.
23. Lu J, Zang WJ, Yu XJ, Jia B, Chorvatova A, Sun L. Effects of postconditioning of adenosine and acetylcholine on the ischemic isolated rat ventricular myocytes. Eur J Pharmacol 549: 133-139, 2006.
24. Mackay K, Mochly-Rosen D. Localization, anchoring, and functions of protein kinase C isozymes in the heart. J Mol Cell Cardiol 33: 1301-1307, 2001.
25. Mullonkal CJ, Toledo-Pereyra LH. Akt in ischemia and reperfusion. J Invest Surg 20: 195-203, 2007.
26. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124-1136, 1986.
27. ATP channel activation during 24 hours of reperfusion (Abstract). J Mol Cell Cardiol 38: 380, 2005.
28. Na HS, Kim YI, Yoon YW, Han HC, Nahm SH, Hong SK. Ventricular premature beat-driven intermittent restoration of coronary blood flow reduces the incidence of reperfusion-induced ventricular fibrillation in a cat model of regional ischemia. Am Heart J 132: 78-83, 1996.
29. Pan TT, Feng ZN, Lee SW, Moore PK, Bian JS. Endogenous hydrogen sulfide contributes to the cardioprotection by metabolic inhibition preconditioning in the rat ventricular myocytes. J Mol Cell Cardiol 40: 119-130, 2006.
30. 2S preconditioning-induced PKC activation regulates intracellular calcium handling in rat cardiomyocytes. Am J Physiol Cell Physiol 294: C169-C177, 2008.
31. Penna C, Cappello S, Mancardi D, Raimondo S, Rastaldo R, Gattullo D, Losano G, Pagliaro P. Post-conditioning reduces infarct size in the isolated rat heart: role of coronary flow and pressure and the nitric oxide/cGMP pathway. Basic Res Cardiol 101: 168-179, 2006.
32. ATP channels trigger cardiac postconditioning through redox signaling. Cardiovasc Res 75: 168-177, 2007.
33. Philipp S, Yang XM, Cui L, Davis AM, Downey JM, Cohen MV. Postconditioning protects rabbit hearts through a protein kinase C-adenosine A2b receptor cascade. Cardiovasc Res 70: 308-314, 2006.
34. Sato H, Jordan JE, Zhao ZQ, Sarvotham SS, Vinten-Johansen J. Gradual reperfusion reduces infarct size and endothelial injury but augments neutrophil accumulation. Ann Thorac Surg 64: 1099-1107, 1997.
35. Sivarajah A, McDonald MC, Thiemermann C. The production of hydrogen sulfide limits myocardial ischemia and reperfusion injury and contributes to the cardioprotective effects of preconditioning with endotoxin, but not ischemia in the rat. Shock 26: 154-161, 2006.
36. Sodha NR, Clements RT, Feng J, Liu Y, Bianchi C, Horvath EM, Szabo C, Sellke FW. The effects of therapeutic sulfide on myocardial apoptosis in response to ischemia-reperfusion injury. Eur J Cardiothorac Surg 33: 906-913, 2008.
37. Staat P, Rioufol G, Piot C, Cottin Y, Cung TT, L'Huillier I, Aupetit JF, Bonnefoy E, Finet G, Andre-Fouet X, Ovize M. Postconditioning the human heart. Circulation 112: 2143-2148, 2005.
38. Sun HY, Wang NP, Halkos M, Kerendi F, Kin H, Guyton RA, Vinten-Johansen J, Zhao ZQ. Postconditioning attenuates cardiomyocyte apoptosis via inhibition of JNK and p38 mitogen-activated protein kinase signaling pathways. Apoptosis 11: 1583-1593, 2006.
39. 2+ overload. Am J Physiol Heart Circ Physiol 288: H1900-H1908, 2005.
40. Szabo C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6: 917-935, 2007.
41. ATP channels by exogenous and endogenous hydrogen sulfide in vascular smooth muscle cells. Mol Pharmacol 68: 1757-1764, 2005.
42. Tissier R, Waintraub X, Couvreur N, Gervais M, Bruneval P, Mandet C, Zini R, Enriquez B, Berdeaux A, Ghaleh B. Pharmacological postconditioning with the phytoestrogen genistein. J Mol Cell Cardiol 42: 79-87, 2007.
43. Tsang A, Hausenloy DJ, Mocanu MM, Yellon DM. Postconditioning: a form of "modified reperfusion" protects the myocardium by activating the phosphatidylinositol 3-kinase-Akt pathway. Circ Res 95: 230-232, 2004.
44. Tsang A, Hausenloy DJ, Yellon DM. Myocardial postconditioning: reperfusion injury revisited. Am J Physiol Heart Circ Physiol 289: H2-H7, 2005.
45. Vinten-Johansen J, Zhao ZQ, Zatta AJ, Kin H, Halkos ME, Kerendi F. Postconditioning-a new link in nature's armor against myocardial ischemia-reperfusion injury. Basic Res Cardiol 100: 295-310, 2005.
46. Wang HC, Zhang HF, Guo WY, Su H, Zhang KR, Li QX, Yan W, Ma XL, Lopez BL, Christopher TA, Gao F. Hypoxic postconditioning enhances the survival and inhibits apoptosis of cardiomyocytes following reoxygenation: role of peroxynitrite formation. Apoptosis 11: 1453-1460, 2006.
47. 2S be the third endogenous gaseous transmitter? FASEB J 16: 1792-1798, 2002.
48. Webb GD, Lim LH, Oh VM, Yeo SB, Cheong YP, Ali MY, El Oakley R, Lee CN, Wong PS, Caleb MG, Salto-Tellez M, Bhatia M, Chan ES, Taylor EA, Moore PK. Contractile and vasorelaxant effects of hydrogen sulfide and its biosynthesis in the human internal mammary artery. J Pharmacol Exp Ther 324: 876-882, 2008.
49. Weber NC, Toma O, Wolter JI, Obal D, Mullenheim J, Preckel B, Schlack W. The noble gas xenon induces pharmacological preconditioning in the rat heart in vivo via induction of PKC-epsilon and p38 MAPK. Br J Pharmacol 144: 123-132, 2005.
50. Yang G, Sun X, Wang R. Hydrogen sulfide-induced apoptosis of human aorta smooth muscle cells via the activation of mitogen-activated protein kinases and caspase-3. FASEB J 18: 1782-1784, 2004.
51. 2S on human aorta smooth muscle cells. FASEB J 20: 553-555, 2006.
52. 2S in rat insulin-secreting cells and the underlying mechanisms. J Physiol 569: 519-531, 2005.
53. Yang XM, Philipp S, Downey JM, Cohen MV. Postconditioning's protection is not dependent on circulating blood factors or cells but involves adenosine receptors and requires PI3-kinase and guanylyl cyclase activation. Basic Res Cardiol 100: 57-63, 2005.
54. Yang XM, Proctor JB, Cui L, Krieg T, Downey JM, Cohen MV. Multiple, brief coronary occlusions during early reperfusion protect rabbit hearts by targeting cell signaling pathways. J Am Coll Cardiol 44: 1103-1110, 2004.
55. Yong QC, Pan TT, Hu LF, Bian JS. Negative regulation of beta-adrenergic function by hydrogen sulphide in the rat hearts. J Mol Cell Cardiol 44: 701-710, 2008.
56. Zatta AJ, Kin H, Lee G, Wang N, Jiang R, Lust R, Reeves JG, Mykytenko J, Guyton RA, Zhao ZQ, Vinten-Johansen J. Infarct-sparing effect of myocardial postconditioning is dependent on protein kinase C signalling. Cardiovasc Res 70: 315-324, 2006.
57. ATP channel opener. EMBO J 20: 6008-6016, 2001.
58. Zhao ZQ, Corvera JS, Halkos ME, Kerendi F, Wang NP, Guyton RA, Vinten-Johansen J. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 285: H579-H588, 2003.
59. Zhao ZQ, Vinten-Johansen J. Postconditioning: reduction of reperfusion-induced injury. Cardiovasc Res 70: 200-211, 2006.
60. Zhi L, Ang AD, Zhang H, Moore PK, Bhatia M. Hydrogen sulfide induces the synthesis of proinflammatory cytokines in human monocyte cell line U937 via the ERK-NF-κB pathway. J Leukoc Biol 81: 1322-1332, 2007.
61. Zhu M, Feng J, Lucchinetti E, Fischer G, Xu L, Pedrazzini T, Schaub MC, Zaugg M. Ischemic postconditioning protects remodeled myocardium via the PI3K-PKB/Akt reperfusion injury salvage kinase pathway. Cardiovasc Res 72: 152-162, 2006.
62. Zhu YZ, Wang ZJ, Ho P, Loke YY, Zhu YC, Huang SH, Tan CS, Whiteman M, Lu J, Moore PK. Hydrogen sulfide and its possible roles in myocardial ischemia in experimental rats. J Appl Physiol 102: 261-268, 2007.